Current Biology
Magazine
of celiac disease. CD4+ pIELs share
differentiation cues with peripheral
Tregs, including TGF- and retinoic acid.
In addition, CD4+ pIELs and intestinal
Tregs appear to play a complementary
role in regulating immune responses
to dietary antigens. However, pro-
inflammatory cytokine-producing CD4+
T cells in the intraepithelial compartment
have also been reported in the mucosa
of patients with celiac disease and
inflammatory bowel disease, suggesting
that CD4+ pIELs may play a detrimental
role in disease as well.
The precise role of each individual
IEL population in disease, whether the
functions of different IEL populations
are complementary or overlapping, and
the heterogeneity in phenotype and
function within each population remain
to be studied in detail.
Where can I find out more?
Cheroutre, H., Lambolez, F., and Mucida, D.
(2011). The light and dark sides of intestinal
intraepithelial lymphocytes. Nat. Rev. Immunol.
11, 445–456.
Denning, T.L., Granger, S.W., Granger, S.,
Mucida, D., Graddy, R., Leclercq, G.,
and Kronenberg, M. (2007). Mouse
TCRalphabeta+CD8alphaalpha intraepithelial
lymphocytes express genes that down-regulate
their antigen reactivity and suppress immune
responses. J. Immunol. 178, 4230–4239.
Di Marco Barros, R., Roberts, N.A., Dart, R.J.,
Vantourout, P., Jandke, A., Nussbaumer, O., and
Hayday, A. (2016). Epithelia use butyrophilin-
like molecules to shape organ-specific  T cell
compartments. Cell 167, 203–218.e17.
Ismail, A.S., Severson, K.M., Vaishnava, S.,
Behrendt, C.L., Yu, X., Benjamin, J.L., and
Hooper, L.V. (2011). Gammadelta intraepithelial
lymphocytes are essential mediators of
host-microbial homeostasis at the intestinal
mucosal surface. Proc. Nat. Acad. Sci. USA 108,
8743–8748.
Kwong, B., and Lazarevic, V. (2014). T-bet
orchestrates CD8 IEL differentiation. Immunity
41, 169–171.
Lefrançois, L., and Puddington, L. (2006). Intestinal
and pulmonary mucosal T cells: local heroes
fight to maintain the status quo. Annu. Rev.
Immunol. 24, 681–704.
Raine, T., Liu, J.Z., Anderson, C.A, Parkes, M.,
and Kaser, A. (2014). Generation of primary
human intestinal T cell transcriptomes reveals
differential expression at genetic risk loci for
immune-mediated disease. Gut 64, 250–259.
Sujino, T., London, M., Hoytema van Konijnenburg,
D.P., Rendon, T., Buch, T., Silva, H. M., and
Mucida, D. (2016). Tissue adaptation of
regulatory and intraepithelial CD4+ T cells
controls gut inflammation. Science 352,
1581–1586.
Vantourout, P., and Hayday, A. (2013). Six-of-
the-best: unique contributions of  T cells to
immunology. Nat. Rev. Immunol. 13, 88–100.
1
Laboratory of Mucosal Immunology, The
Rockefeller University, New York, NY, USA.
2
Laboratory of Translational Immunology,
University Medical Center Utrecht, The
Netherlands.
*E-mail: mucida@rockefeller.edu
Primer pheromones. The first identification of
a pheromone was not published until
Pheromones 1959: it had taken Adolf Butenandt
and his team 20 years and required
material from half a million female silk
Tristram D. Wyatt moths. Today, a single female moth’s
secretion might be sufficient, analyzed
The reality of invisible chemical by gas-chromatography–mass-
signals, pheromones, between spectrometry (GC-MS) combined
members of the same species with electrophysiological recordings
was recognized long before they from a male moth’s antenna to
could be identified. Charles Darwin detect the active components of the
proposed that the breeding season pheromone blend. Many pheromones,
sexual smells of male crocodiles, perhaps most, consist of a particular
goats and other animals, too, could combination of molecules, not a single
have evolved by sexual selection molecule.
of the smelliest males through Butenandt used the wing fluttering
female choice. But it’s not just sex. response of the male silk moth as
We now know that pheromones the bioassay to track the female sex
are used by species all across the pheromone activity in his solvent
animal kingdom, in every habitat, fractionations and to later confirm that
and in a wide range of biological the synthesized molecule, bombykol,
contexts, from trail, alarm, and queen was indeed the pheromone. Such
pheromones in social insects to the bioassays, repeatable experiments
mammary pheromone produced designed to measure a biological
by mother rabbits. Pheromones response, are still an essential part of
have provided fascinating examples pheromone identification. Without this
of signal evolution. In some systematic approach, no claim that a
model organisms, such as moths, molecule or combination of molecules
Drosophila, Caenorhabditis elegans, is a pheromone is credible (Box 1).
and Mus musculus, a complete Many bioassays measure a
signaling system can be genetically behavioural response as in the silk
dissected, from the enzymes moth or the suckling of a rabbit pup
producing pheromones, perception in response to the rabbit mammary
by chemosensory receptors, through pheromone, 2-methylbut-2-enal.
to the neural circuits processing the Other pheromones need different
signals. kinds of bioassays as they have
The challenge for scientists physiological (‘primer’) effects. Many
historically was that individual animals pheromones, such as male tilapia
typically release vanishingly small urinary pheromones (Figure 1) and
micro- or pico-gram quantities of honeybee alarm pheromone, have
Box 1. Pheromones: an operational definition.
1. The synthesized molecule/combination of molecules should elicit the same
response as the natural stimulus in the bioassay. This is the fundamental basis for the
designation of a pheromone.
2. It should act in this way at natural concentrations. Concentration is important. At
high concentrations, spurious results may occur as non-pheromones may stimulate
receptors.
3. For multicomponent pheromones, experiments should demonstrate that all
compounds in the combination are necessary and sufficient to elicit the full
response.
4. Only this molecule or the proposed combination of molecules elicits the effect
(unlike other similar molecules or combinations that the animal would normally
encounter).
5. There should be a credible pathway for the pheromone signal to have evolved by
direct or kin selection. In evolutionary terms, to be a signal, both the emission and
reception of the pheromone signal should have evolved for a particular function.
Adapted from Wyatt, T.D. (2014). Pheromones and Animal Behavior: Chemical Signals and
Signatures, 2 edn. (Cambridge: Cambridge University Press).
Current Biology 27, R731–R745, August 7, 2017 © 2017 Elsevier Ltd. R739
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Dominant male -
few exceptions, learning underlies all
O
O

Increased urination HO
HO O
H
OH
OH
recognition.
during courtship HO
-
O OH
O
O

H
H
H It is worth separating the concepts
HO H OH
O

Male urine vehicle for H

H O
HO
OH
of pheromones and signature mixtures
H
5-Pregnane-3,17,20-triol 3-glucuronate (it was a mistake in my 2003 book to
5-Pregnane-3,17,20-triol 3-glucuronate
OH Olfactory receptor(s)
combine them). It is precisely because
OH individuals have different odour
-
O H profiles that these can be learnt and
*

Brain-pituitary-
O

gonadal axis
O H H used to distinguish different animals.
HO O
HO
OH H Examples abound, from a mother
sheep distinguishing her lambs from
OH
OH others, a monogamous prairie vole
- H (Microtus ochrogaster) recognizing its
*O O
O H H partner by smell, or, in many species,
HO O
HO
OH H Ovary avoiding close kin when choosing a
17,20-P surge
oocyte maturation
mate. Similarly, in social insects such
as ants, bees, wasps, and termites,
the differences in chemical profile
between colonies allow animals to
Spawning synchrony distinguish nest-mates and non-nest-
Current Biology
mate conspecifics.
Social insect workers do not
Figure 1. Male tilapia sex pheromones have multiple effects. reproduce in the presence of queen
Sex pheromones in the urine of dominant male Mozambique tilapia (Oreochromis mossambicus)
pheromones (Figure 2). Candidate
deter subordinate males, attract females and prime ovulation in females. Two steroid glucuronates
(5-pregnane-3,17,20-triol 3-glucuronate and its 20-epimer) are produced in large quantities queen pheromones in ants, bees, and
by dominants and are the most potent urinary odorants to females. They act via (a) specific and wasps could be identified because
common olfactory receptor(s) on the females’ endocrine axis, stimulating production and release they were molecules that all queens
of 17,20-P, the major oocyte maturation-inducing hormone in teleost fishes. This leads to the in a species shared and which
ripening of the oocytes and (likely) synchronizes spawning. (From Keller-Costa, T. et al. (2015). workers produced little of. The queen
Chemical communication in cichlids: a mini-review. Gen. Comp. Endocrinol. 221, 64–74.)
pheromone molecule(s) appeared in the
gas chromatogram traces as constant
both immediate ‘releaser’ effects and interfered with by an experimenter, peaks in all queens, overlaid on a
longer lasting primer effects. In the previously invisible dependencies can complex colony odour background of
honey bee this is reflected in changes be revealed. For example, honeybee cuticular hydrocarbons, highly variable
in gene activity in the bee’s antennal workers need early exposure to queen between colonies. The candidate
lobe. For many hours after exposure mandibular pheromone in order to be molecules could then be tested in
to alarm pheromone, honeybees are attracted to it when they attend the bioassays to see if they reproduced
more likely to attack intruders. queen as older workers. the queen pheromone’s physiological
Pheromones elicit stereotyped effects on the workers of that species.
behavioural and/or physiological Pheromones and individual or In mammals, which have individual
responses but these are modulated by colony odours odour profiles easily as complex as
context, time of day, and many other Pheromones are the same in all social insect colony odours, early
factors including the receiver’s genetics, sexually mature males, for example, researchers despaired of finding
age, sex, hormonal state, dominance of a species. It is the consistency pheromones. GC analysis of
status, and recent experience. For in these molecules between mammal secretions from skin glands
example, male Agrotis moths do not individual males in a population showed they contained hundreds
respond to female sex pheromone which allows them to be identified of molecules, with large variations
for up to 24 hours after mating. Even as a pheromone. Some males may in composition between different
though pheromone still stimulates the produce more of the pheromone individuals of the same species. As
olfactory sensory neurons in the male and thus may be more attractive to with the queen pheromones, the tactic
moth’s antennae, the brain response is females: well-fed male voles with high to track down pheromones against
blocked until enough time has elapsed testosterone levels produce more this background was to look for
for the male to have replenished pheromone. Pheromones are one molecules that consistently appeared,
his accessory protein stores to go kind of semiochemical, chemicals for example, in the chemical profile
with his sperm. Male hamsters only giving information. Another kind of of males but not females. Since the
respond to female pheromone if they semiochemical, signature mixtures, production of many male pheromones
are well fed, giving them sufficiently are the basis of individual recognition in mammals is under androgen
high blood testosterone levels in their based on learning the different hormone control, the chemical profiles
hypothalamus. chemical profiles of individuals, of intact and castrated males could
While, typically, pheromones do not allowing familiar and unfamiliar also be compared. This ‘subtractive
need to be learnt, if development is animals to be distinguished. With approach’ was used recently to track

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down candidate molecules for a male
goat pheromone. Similar approaches
have also been used to identify large
molecule pheromones in male mice,
such as the endocrine-gland-secreting
peptide 1 (ESP1) from the tear gland
and the major urinary protein (MUP20),
known as darcin.
Darcin provides a good example of
the distinction between pheromones
and individual odours. Darcin is
secreted in the urine that dominant
male mice use to mark territory
signposts. Females, attracted by
volatile urine pheromones, sniff the
urine into their second nose, the
vomeronasal organ (VNO), where
darcin, an involatile pheromone, is
detected. Darcin prompts the female
to remember the location of the
signpost and also the individual odour
of the male. She will seek out the male
territory owner and mate with him,
recognizing him by his individual odour.
Pheromone production
Pheromones are typically secreted
by specialized glands or tissues.
For example, female moths have a
pheromone gland at the end of their
abdomen. Rodents have a wide
variety of skin glands as well as large
and small pheromone molecules
delivered in their urine. In some
species, pheromones are derived or
modified from other sources: tiger
moth caterpillars sequester poisons
from their milkweed food plants and
as adults, males metabolise some of
these pyrrolizidine alkaloid poisons
into volatile pheromones, attractive to
females and indicative of the size of
poison gift they will transfer along with
sperm at mating. Tropical euglossine
orchid bee males collect their
pheromones as a ‘take-away’ from a
species-specific set of orchid flowers.
Pheromones may also be produced by
the activity of bacterial symbionts as
in the case of, for example, guaiacol
(2-methyoxyphenol), which affects
phase-change in Locusta migratoria.
Which molecules evolve into
pheromones?
A very wide range of molecules
are used as pheromones, covering
every chemical dimension of
structure, functional group, size and
combination, and limited only by the
range of molecules organisms can
Reproductive division of labor
Selection of eggs to be
reared or cannibalized
Aggressive policing and
Control of queen choice of reproductive(s)
rearing and adoption by workers
Direct inhibition of
worker/subordinate
reproduction
Regulation of task
allocation and
learning in Inhibition of aggression
workers towards the primary
reproductive
Self-regulation of
oviposition by
reproductive
Brood-borne queen
Colony regulation pheromones
Queen-borne queen
pheromones
Current Biology
Figure 2. Functions of queen pheromones in social insects.
This illustration features a queen ant, but it could be a queen bee, wasp, or termite. Such func-
tions have been demonstrated experimentally in at least one species but not necessarily all taxa.
Cuticular hydrocarbon queen pheromones have evolved independently in the different lineages
of social Hymenoptera. Inset: main component of the queen pheromone of the ant Lasius niger,
3-methylhentriacontane. (Figure from Holman, L. (2010). Queen pheromones: the chemical crown
governing insect social life. Commun. Integr. Biol. 3, 558–560 with permission from Luke Holman.)
produce or obtain. This range reflects turn, females would be selected to
the ways that molecules evolve into secrete more of these molecules to
pheromone signals. Any molecule can function as a pheromone signal. This
potentially evolve into a pheromone. evolved production and reception of
There are probably two main the signal distinguishes pheromone
routes for pheromones to evolve: signals from cues (information used
the first is from molecular cues by the receiver but not evolved as a
associated with a physiological state signal by the emitter, as in the case
in the emitter. This transition from of mosquitoes attracted to the smells
cue to pheromone is facilitated by we give off just by being alive).
the broad sensitivity of olfactory A second evolutionary route for
systems (below). The discovery that pheromones is by exploitation of pre-
fish female sex pheromones are existing sensitivities in the receiver
hormones or chemical variations to molecules associated with other
on them can be explained by an functions such as food finding. Male
evolutionary scenario starting with moth pheromones used in the final
‘eavesdropping’. It starts with stages of courtship in many moth
selection on males for sensitivity for families tend to be similar to plant
these molecular cues leaking from molecules that females are sensitive
females about to lay eggs. Those to for host-plant location. Males
mutant males with more olfactory would have been selected to produce
receptors for these hormones the molecules that females already
would get to the females first and detect. Now that it has evolved into
their offspring would dominate a signal, females will not mate with
subsequent generations. There males which do not release the
would be selection on male olfactory correct species-specific pheromone
receptors for increased specificity to during courtship.
reduce false alarms, and an increase The molecules used by a given kind
in expression to raise sensitivity. In of animal can often be understood
Current Biology 27, R731–R745, August 7, 2017 R741
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activated, indicating all pheromone

O CH3
Z12-14:OAc components are present in the right
H3 C O
O
ratios, and there are no pheromone
H3 C O CH3 E12-14:OAc molecules characteristic of other
CH3
species.
H3 C O Z11-14:OAc In mammals, which type of
O O chemosensory receptors/olfactory
H3 C O CH3 E11-14:OAc sensory neuron has been coopted to
detect the pheromone depends on
HO CH3 E11-14:OH the molecule: volatile pheromones
CH3
may be detected by chemosensory
Z9-14:OAc
H3 C O
neurons in either the main olfactory
O system or accessory olfactory system

ia r

lis

is
s
z a p. n i

fur e v i
gu E
O. ula is E
O. pulalis Z
sc bil Z

v
gu e a

ali

ali

nn
O. liae
(Figure 4). Protein pheromones such

ca
z a lis
O. nu lis

ze

r
ap a l

t
ipe
a a

na
Proportion in blend

lus
as ESP1, ESP22, and darcin are likely
s c bil

O.
s

lat
pa
O . . nu

detected exclusively by VR2 receptors

O.

O.
O.
O

of the vomeronasal system whereas

100 50 20 5 1 sulphated steroid pheromones are
Current Biology
detected by VR1 receptors. Important
Figure 3. Multicomponent pheromones offer species specificity. amines are detected by trace amine-
Most pheromones are a specific blend of molecules. Different corn borer moth Ostrinia species associated receptors (TAARs). In
share different combinations and concentrations of six molecules. Inset: adult female European mammals, many receptors have not
corn borer O. nubilalis. Photo: John Obermeyer, Purdue Extension Entomology. (Adapted from been matched to their ligands.
Lassance, J.M. et al. (2013). Functional consequences of sequence variation in the pheromone Drosophila melanogaster is
biosynthetic gene pgFAR for Ostrinia moths. Proc. Natl. Acad. Sci. USA 110, 3967–3972.)
something of an anomaly with a
much greater role for taste (gustatory)
in terms of function, habitat, likely in female signal are matched by receptors (via non-glomerular
evolution, and phylogenetic history. changes in the male pheromone pathways) along with olfactory
For example, ant alarm pheromones receptors and/or neural circuits for receptors for processing some
are often related to that species’ processing the sex pheromone. Carp pheromones. Sex-specific neural
venoms, and are small volatile of different species avoid interspecies circuits integrate sensory inputs
molecules such as formic acid (MW matings by distinguishing different from the different chemosensory
46), quick to reach fellow nestmates multicomponent pheromones. systems plus visual and song inputs.
and to rapidly disperse when the alert Across nematode species, different The distinction between olfactory
is over. By contrast, hyena anal gland combinations of a diversity of and taste receptors is less clear in
secretions contain relatively involatile ascarosides, a nematode-specific crustaceans but the importance of
high molecular weight molecules family of glycolipids, act as species- pheromones is well established,
for long lasting marks for territory specific sex and other pheromones. though few have been chemically
marking. Underwater, pheromones identified.
can be small as the unusual amino Pheromone perception Some pheromones bypass the
acid L-kynurenine used by masu Across the animal kingdom, as a conventional chemosensory systems
salmon as a female sex pheromone rule, pheromones are detected by and instead act on receptors on
or as large as proteins, if charged chemoreceptors of the olfactory other neurons or on cells in tissues
and soluble. For example, the sex system(s). In both insects and themselves. These pheromones
pheromones of the sea slug Aplysia vertebrates, olfactory sensory neurons have been called allohormone
are the proteins attractin, enticin, which carry the same chemoreceptor pheromones because they act like
seductin, and temptin. converge on the same glomerulus hormones outside the sender’s
During speciation, changes in (whether this organization has arisen body. For example, honeybee
sex pheromones commonly form independently is still unclear). This larvae destined to be queens
one basis of pre-mating isolation. glomerular organization is the basis are fed exclusively on royal jelly,
This may explain the chemosignal of the combinatorial processing which contains a glycoprotein
differences in major urinary proteins of general odorants (of food and allohormone pheromone, royalactin.
and androgen binding proteins in habitat etc). What distinguishes This acts on a fat body signaling
Mus musculus subspecies in hybrid pheromones is the selection for high cascade, resulting in raised juvenile
zones. Pheromones commonly specificity of their receptors, which hormone levels. When development
consist of particular combinations leads to the phenomenon of ‘labelled is complete, queens are very
of molecules. Different species of lines’, activating one glomerulus different from workers: they are
Ostrinia corn borer moths have added per pheromone component. In larger, have different neural circuits
and lost molecules from their female male moths, interneurons will only and behaviours, have functioning
pheromone blends, offering variations initiate a behavioural response if the reproductive systems, and will live
on a theme (Figure 3). These changes right combination of glomeruli are ten times as long. In some species,

R742 Current Biology 27, R731–R745, August 7, 2017

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CP
MC
GL
OSN
AOB
MOB
GG
SO MOE
VNO VSN
BV
Current Biology
Figure 4. Pheromone perception in mice.
In the mouse, pheromones are processed by
both its main olfactory and accessory olfac-
tory systems as well as other chemosensory
subsystems, including the septal organ (SO),
and Grueneberg ganglion (GG). Chemical sig-
natures are also processed by both the main
and accessory olfactory systems. Olfactory
sensory neurons (OSN) in the main olfactory
epithelium (MOE) project to glomeruli in the
main olfactory bulb (MOB) and those express-
ing the same olfactory receptor converge on
a single glomerulus (GL). Mitral cells (MC) ex-
tend an apical dendrite into adjacent glomeruli
and extend axons to the forebrain. Vomerona-
sal sensory neurons (VSN) extend axons from
the vomeronasal organ (VNO) to the accessory
olfactory bulb (AOB). BV; blood vessel, CP;
cribiform plate. (From Spehr, M. et al. (2006).
Parallel processing of social signals by the
mammalian main and accessory olfactory sys-
tems. Cell. Mol. Life Sci. 63, 1476–1484 with
permission from Springer.)
hormones or other molecules are
transferred along with the male’s
sperm to the female when mating,
causing females to reject other
males. These molecules include
prostaglandins in the semen of the
red-sided garter snake Thamnophis
sirtalis parietalis and sex peptides in
the semen of D. melanogaster.
Practical applications
Pheromones have fulfilled their early
promise for non-toxic pest control.
For example, with sufficient synthetic
female sex pheromone released
into an apple orchard, male codling
moths cannot find the real females
to fertilize their eggs (so there are
fewer caterpillars, which cause the
damage). In contrast to broadly
toxic pesticides, the specificity of
non-toxic sex pheromones means
that environmental impacts are
minimised — predators such as
spiders and carabid beetles are left
unaffected. However, the species-
specificity of sex pheromones
increases costs as pheromone
control has to be developed for
each pest. Despite these challenges
for commercialization, more than
10 million hectares are protected
annually using pheromones.
So far, pest moths and beetles have
been the main targets. In the future,
nematodes and insect vectors of
disease might be managed by their
pheromones. Lampreys which ravage
Great Lake fisheries might soon be
lured into traps by their pheromones.
Rodent pheromones might one day
replace toxic rodenticides.
Eavesdropping and deception
Broadcast signals like pheromones
can be ‘eavesdropped’. When
researchers in California put out traps
to fieldtest bark beetle aggregation
pheromones (which attract
conspecifics of both sexes), they
were surprised to also catch 600,000
predatory beetles. It was later found
that the predators had evolved
olfactory receptors highly sensitive to
their prey’s pheromones.
Similarly, other species can
counterfeit signals. The female bolas
spider lures male moths within reach
of her sticky ‘bolas’ by synthesising
convincing moth pheromones. She
produces different pheromone
blends through the night to match
the different peak flight times of her
victim moth species. Plants too
can use chemical trickery. Orchids
have flowers that mimic the look and
pheromones of a particular female
bee or wasp species. The male insect
attempts to mate, picks up a pollen
package, and having been fooled
once, is fooled again, delivering the
package to a second orchid of the
same species.
Do humans have pheromones?
This ever interesting question remains
unresolved. Sadly, though widely
offered for sale, the putative human
sex ‘pheromones’ androstadienone
and estratetraenol (and androstenol
and androstenone) have never
been properly demonstrated to be
pheromones. This has not stopped
many studies claiming to show such
Current Biology 27, R731–R745, August 7, 2017
effects, likely to be false positives
since there are no reasons to
even suspect these molecules are
pheromones. However, there might
be a human mammary pheromone,
suggested by the response of
human babies to secretions from
any lactating mother, not just their
own. Babies suck in response to
secretions from the areola gland
around the nipple. These are being
chemically investigated and, if the
early observations are substantiated,
could lead to the identification of the
first human pheromone.
FURTHER READING
Allison, J.D., and Cardé, R.T. (2016). Pheromone
Communication in Moths: Evolution, Behavior
and Application (Berkeley, CA: University of
California Press).
Bear, D.M., Lassance, J.-M., Hoekstra, H.E, and
Datta, S.R. (2016). The evolving neural and
genetic architecture of vertebrate olfaction.
Curr. Biol. 26, R1039–R1049.
Breithaupt, T., and Thiel, M. (2011). Chemical
Communication in Crustaceans (New York:
Springer).
Kohl, J., Huoviala, P., and Jefferis, G.S. (2015).
Pheromone processing in Drosophila. Curr.
Opin. Neurobiol. 34, 149–157.
Leighton, D.H., and Sternberg, P.W. (2016).
Mating pheromones of Nematoda: olfactory
signaling with physiological consequences.
Curr. Opin. Neurobiol. 38, 119–124.
Liberles, S.D. (2014). Mammalian pheromones.
Annu. Rev. Physiol. 76, 151–175.
Logan, D.W. (2015). The complexity of
pheromone-mediated behaviour in mammals.
Curr. Opin. Behav. Sci. 2, 96–101.
Murata, K., Tamogami, S., Itou, M., Ohkubo, Y.,
Wakabayashi, Y., Watanabe, H., Okamura, H.,
Takeuchi, Y., and Mori, Y. (2014). Identification
of an olfactory signal molecule that activates
the central regulator of reproduction in goats.
Curr. Biol. 24, 681–686.
Oi, C.A., van Zweden, J.S., Oliveira, R.C.,
Van Oystaeyen, A., Nascimento, F.S.,
and Wenseleers, T. (2015). The origin and
evolution of social insect queen pheromones:
novel hypotheses and outstanding problems.
Bioessays 37, 808–821.
Renou, M. (2014). Pheromones and general
odor perception in insects. In Neurobiology
of Chemical Communication, C. Mucignat-
Caretta, ed. (Boca Raton, FL: CRC Press),
pp. 23–56.
Sorensen, P.W., and Wisenden, B.D. (2015). Fish
Pheromones and Related Cues (Hoboken:
John Wiley).
Touhara, K. (2013). Pheromone Signaling:
Methods and Protocols (New York, NY:
Humana Press).
Wyatt, T.D. (2014). Pheromones and Animal
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Department of Zoology, University of
Oxford, Oxford OX1 3PS, UK.
E-mail: tristram.wyatt@zoo.ox.ac.uk
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